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. 1997 Oct 1;504(Pt 1):153–168. doi: 10.1111/j.1469-7793.1997.153bf.x

Fast (mainly 30-100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials.

I Timofeev 1, M Steriade 1
PMCID: PMC1159944  PMID: 9350626

Abstract

1. Intracellular recordings from 216 thalamocortical (TC) neurones in the ventrolateral (VL) nucleus of intact-cortex and decorticated cats under ketamine-xylazine anaesthesia revealed spontaneously occurring fast oscillations (mainly 30-100 Hz) in 86% of investigated cells. The fast depolarizing events consisted of excitatory postsynaptic potentials (EPSPs), giving rise to fast prepotentials (FPPs) in 22% of neurones, which eventually lead to full-blown action potentials. The frequency of fast events changed by factors of 2-5 in periods as short as 0.3-1.0 s. 2. The spontaneous oscillations were similar to responses evoked in VL relay neurones by stimuli to the afferent cerebellofugal axons in brachium conjunctivum (BC) and were strikingly reduced or abolished after electrolytic lesion of BC axons. 3. The amplitude and duration of fast depolarizing events were significantly reduced during the descending phase of the inhibitory postsynaptic potentials (IPSPs) in TC cells, related to spontaneous spindles or evoked by local thalamic stimulation. 4. Averaged field potentials recorded from motor cortex and triggered by EPSPs and/or action potentials of intracellularly recorded VL cells demonstrated that both spontaneous and BC-evoked fast depolarizations in VL relay neurones were coherent with fast rhythms in cortical area 4. 5. These results show that, in addition to the thalamic and cortical generation sites of the fast (so-called gamma) oscillations, prethalamic relay stations, such as deep cerebellar nuclei, are major contributors to the induction of fast rhythms which depend on the depolarization of thalamic and cortical neurones and which represent a hallmark of brain activation patterns.

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Selected References

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  1. Amzica F., Neckelmann D., Steriade M. Instrumental conditioning of fast (20- to 50-Hz) oscillations in corticothalamic networks. Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1985–1989. doi: 10.1073/pnas.94.5.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bal T., von Krosigk M., McCormick D. A. Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. J Physiol. 1995 Mar 15;483(Pt 3):641–663. doi: 10.1113/jphysiol.1995.sp020612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Contreras D., Steriade M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci. 1995 Jan;15(1 Pt 2):604–622. doi: 10.1523/JNEUROSCI.15-01-00604.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Crunelli V., Haby M., Jassik-Gerschenfeld D., Leresche N., Pirchio M. Cl- - and K+-dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. J Physiol. 1988 May;399:153–176. doi: 10.1113/jphysiol.1988.sp017073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Deschênes M., Paradis M., Roy J. P., Steriade M. Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. J Neurophysiol. 1984 Jun;51(6):1196–1219. doi: 10.1152/jn.1984.51.6.1196. [DOI] [PubMed] [Google Scholar]
  6. Ghose G. M., Freeman R. D. Oscillatory discharge in the visual system: does it have a functional role? J Neurophysiol. 1992 Nov;68(5):1558–1574. doi: 10.1152/jn.1992.68.5.1558. [DOI] [PubMed] [Google Scholar]
  7. Jahnsen H. Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol. 1986 Mar;372:129–147. doi: 10.1113/jphysiol.1986.sp016001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol. 1984 Apr;349:205–226. doi: 10.1113/jphysiol.1984.sp015153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Llinás R., Mühlethaler M. Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol. 1988 Oct;404:241–258. doi: 10.1113/jphysiol.1988.sp017288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Llinás R., Ribary U. Coherent 40-Hz oscillation characterizes dream state in humans. Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2078–2081. doi: 10.1073/pnas.90.5.2078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Maekawa K., Purpura D. P. Properties of spontaneous and evoked synaptic activities of thalamic ventrobasal neurons. J Neurophysiol. 1967 Mar;30(2):360–381. doi: 10.1152/jn.1967.30.2.360. [DOI] [PubMed] [Google Scholar]
  12. McCormick D. A., Pape H. C. Acetylcholine inhibits identified interneurons in the cat lateral geniculate nucleus. Nature. 1988 Jul 21;334(6179):246–248. doi: 10.1038/334246a0. [DOI] [PubMed] [Google Scholar]
  13. Mouginot D., Gähwiler B. H. Characterization of synaptic connections between cortex and deep nuclei of the rat cerebellum in vitro. Neuroscience. 1995 Feb;64(3):699–712. doi: 10.1016/0306-4522(94)00456-f. [DOI] [PubMed] [Google Scholar]
  14. Neuenschwander S., Singer W. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature. 1996 Feb 22;379(6567):728–732. doi: 10.1038/379728a0. [DOI] [PubMed] [Google Scholar]
  15. Nuñez A., Amzica F., Steriade M. Intrinsic and synaptically generated delta (1-4 Hz) rhythms in dorsal lateral geniculate neurons and their modulation by light-induced fast (30-70 Hz) events. Neuroscience. 1992 Nov;51(2):269–284. doi: 10.1016/0306-4522(92)90314-r. [DOI] [PubMed] [Google Scholar]
  16. Nuñez A., Curró Dossi R., Contreras D., Steriade M. Intracellular evidence for incompatibility between spindle and delta oscillations in thalamocortical neurons of cat. Neuroscience. 1992;48(1):75–85. doi: 10.1016/0306-4522(92)90339-4. [DOI] [PubMed] [Google Scholar]
  17. Pape H. C., McCormick D. A. Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus. Neuroscience. 1995 Oct;68(4):1105–1125. doi: 10.1016/0306-4522(95)00205-w. [DOI] [PubMed] [Google Scholar]
  18. Pedroarena C., Llinás R. Dendritic calcium conductances generate high-frequency oscillation in thalamocortical neurons. Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):724–728. doi: 10.1073/pnas.94.2.724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pinault D., Deschênes M. The origin of rhythmic fast subthreshold depolarizations in thalamic relay cells of rats under urethane anaesthesia. Brain Res. 1992 Nov 13;595(2):295–300. doi: 10.1016/0006-8993(92)91063-k. [DOI] [PubMed] [Google Scholar]
  20. Plenz D., Kitai S. T. Generation of high-frequency oscillations in local circuits of rat somatosensory cortex cultures. J Neurophysiol. 1996 Dec;76(6):4180–4184. doi: 10.1152/jn.1996.76.6.4180. [DOI] [PubMed] [Google Scholar]
  21. Sawyer S. F., Young S. J., Groves P. M., Tepper J. M. Cerebellar-responsive neurons in the thalamic ventroanterior-ventrolateral complex of rats: in vivo electrophysiology. Neuroscience. 1994 Dec;63(3):711–724. doi: 10.1016/0306-4522(94)90517-7. [DOI] [PubMed] [Google Scholar]
  22. Steriade M., Amzica F., Contreras D. Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci. 1996 Jan;16(1):392–417. doi: 10.1523/JNEUROSCI.16-01-00392.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Steriade M. Ascending control of thalamic and cortical responsiveness. Int Rev Neurobiol. 1970;12:87–144. doi: 10.1016/s0074-7742(08)60059-8. [DOI] [PubMed] [Google Scholar]
  24. Steriade M., Contreras D., Amzica F., Timofeev I. Synchronization of fast (30-40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks. J Neurosci. 1996 Apr 15;16(8):2788–2808. doi: 10.1523/JNEUROSCI.16-08-02788.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Steriade M., Dossi R. C., Paré D., Oakson G. Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4396–4400. doi: 10.1073/pnas.88.10.4396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Steriade M., Iosif G., Apostol V. Responsiveness of thalamic and cortical motor relays during arousal and various stages of sleep. J Neurophysiol. 1969 Mar;32(2):251–265. doi: 10.1152/jn.1969.32.2.251. [DOI] [PubMed] [Google Scholar]
  27. Steriade M. Two channels in the cerebellothalamocortical system. J Comp Neurol. 1995 Mar 27;354(1):57–70. doi: 10.1002/cne.903540106. [DOI] [PubMed] [Google Scholar]
  28. Timofeev I., Contreras D., Steriade M. Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat. J Physiol. 1996 Jul 1;494(Pt 1):265–278. doi: 10.1113/jphysiol.1996.sp021489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Timofeev I., Steriade M. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J Neurophysiol. 1996 Dec;76(6):4152–4168. doi: 10.1152/jn.1996.76.6.4152. [DOI] [PubMed] [Google Scholar]
  30. Williams S. R., Turner J. P., Anderson C. M., Crunelli V. Electrophysiological and morphological properties of interneurones in the rat dorsal lateral geniculate nucleus in vitro. J Physiol. 1996 Jan 1;490(Pt 1):129–147. doi: 10.1113/jphysiol.1996.sp021131. [DOI] [PMC free article] [PubMed] [Google Scholar]

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